Alpha proteobacterial ancestry of the [Fe-Fe]-hydrogenases in anaerobic eukaryotes
© The Author(s). 2016
Received: 9 June 2016
Accepted: 21 July 2016
Published: 30 July 2016
Eukaryogenesis, a major transition in evolution of life, originated from the symbiogenic fusion of an archaea with a metabolically versatile bacterium. By general consensus, the latter organism belonged to α proteobacteria, subsequently evolving into the mitochondrial organelle of our cells. The consensus is based upon genetic and metabolic similarities between mitochondria and aerobic α proteobacteria but fails to explain the origin of several enzymes found in the mitochondria-derived organelles of anaerobic eukaryotes such as Trichomonas and Entamoeba. These enzymes are thought to derive from bacterial lineages other than α proteobacteria, e.g., Clostridium - an obligate anaerobe. [FeFe]-hydrogenase constitues the characteristic enzyme of this anaerobic metabolism and is present in different types also in Entamoeba and other anaerobic eukaryotes. Here we show that α proteobacteria derived from metagenomic studies possess both the cytosolic and organellar type of [FeFe]-hydrogenase, as well as all the proteins required for hydrogenase maturation. These organisms are related to cultivated members of the Rhodospirillales order previously suggested to be close relatives of mitochondrial ancestors. For the first time, our evidence supports an α proteobacterial ancestry for both the anaerobic and the aerobic metabolism of eukaryotes.
Reviewers: This article was reviewed by William Martin and Nick Lane, both suggested by the Authors.
KeywordsEukaryogenesis Anaerobic metabolism [FeFe]-hydrogenase Mitochondria Bioenergetics
Mounting interest is arising on eukaryogenesis, a major transition in evolution which most likely originated from a symbiogenic event between an archaea and a metabolically versatile bacterium [1, 2]. The archaean partner of this symbiogenic event appears to be related to the Loki organisms recently discovered in deep ocean vents . In contrast, the definition of the bacterial lineage for the other prokaryotic partner of eukaryogenesis remains unclear and controversial [2–9]. Recent analysis of major bioenergetic systems shared by bacteria and mitochondria suggests that a subset of extant α proteobacteria could be related to the ancestral lineage from which mitochondrial organelles of eukaryotic cells evolved [4, 8, 10]. However, biochemical and phylogenetic evidence emerged from the study of anaerobic eukaryotes seriously challenges the possibility that α proteobacterial organisms may be the ancestors also for the anaerobic metabolism of eukaryotes such as Trichomonas and Entamoeba [11, 12].
Trichomonas, Entamoeba and other eukaryotes adapted to anaerobic conditions possess Mitochondria Related Organelles (MRO [3, 12–14]) carrying out reactions of anaerobic metabolism that are typical of obligate anaerobes such as Clostridium, rather than α proteobacteria [12–19]. [FeFe]-hydrogenase constitutes the distinctive enzyme of this anaerobic metabolism and is present in different types [12–19], both in MRO and the cytosol of anaerobic eukaryotes such as Mastigamoeba . The wide molecular variations of [FeFe]-hydrogenases [11, 12, 15–19] are present in many obligate anaerobes, in particular Clostridiales, Thermotogales and δ proteobacteria [12–19]; only a few facultative anaerobic α proteobacteria such as Rhodospirillum rubrum have similar hydrogenases, but not the maturases required for their biogenesis . Consequently, it has been concluded that the eukaryotic types of this enzyme have been laterally acquired from bacterial lineages other than α proteobacteria, along various elements of anaerobic metabolism [11–13, 16–19]. Clearly, this conclusion undermines the hypothesis that a single α proteobacterium could have been the ancestor of both the anaerobic and the anaerobic metabolism of eukaryotes [1, 3, 6, 8].
Here we show that some α proteobacterial organisms found in metagenomic analysis of human microbiota  possess the two major types of eukaryotic [FeFe]-hydrogenases, as well as all genes needed for its assembly and maturation. Moreover, we report that relatives of photosynthetic Rhodospirillum  and methanotrophic α proteobacterial previously indicated as possible relatives of the mitochondrial ancestors [10, 22] possess a major type of eukaryotic [FeFe]-hydrogenases that could be the ancestor also of the hydrogenase-related Nar1 protein, which is involved in the biogenesis of Fe-S clusters of all eukaryotes . Our findings thus rectify previous conclusions, strengthening the possibility that eukaryotes inherited also their anaerobic metabolism from a single α proteobacterial ancestor.
Results and discussion
Some α proteobacteria possess all the maturases for [FeFe]-hydrogenase
Proteins of anaerobic metabolism in cultivated and uncultivated α proteobacteria
Accession number of indicated proteins
metagenome assembly, refined
Acetobacter MGS:igc0867 a , formerly CAG:977
Fdsα/NuoG-like, type M3 [FeFe]-hydrogenase
M2 & M3 derivatives
type A [FeFe]-hydrogenase
Yes, ≥ 2
Yes, ≥ 2
Yes, ≥ 2
Yes, ≥ 5
Yes, ≥ 1
Yes, ≥ 2
Yes, ≥ 3
We found that one gene for the long form of [FeFe]-hydrogenase in Acetobacter CAG:977 and Azospirillum sp. CAG:239 is associated with genes coding homologues of two redox subunits of respiratory complex I, which form the NADH-reacting module of the enzyme: NuoE and NuoF (Table 1, cf. [31–34]). The eukaryotic orthologs of these proteins are the 24 and 51 kDa subunits of mitochondrial complex I that are always coded by nuclear DNA, while the rest of complex I subunits is encoded by mtDNA in several protists [5, 32, 34]. The same proteins are found in the hydrogenosomes - a specialised form of MRO  - of Trichomonas  and Sawyeria, an anaerobic Heterolobosea , which lack complex I . The gene cluster containing the long form of [FeFe]-hydrogenase and NuoEF homologues in the organisms identified from metagenomic analysis  resembles the hymABC operon described in Clostridiales [36, 37] (Table 1). In turn, this operon clearly derives from the Fds operon of NAD-dependent formate dehydrogenase , from which the NADH-reacting module of respiratory complex I originated [32, 34]. Of note, the genome of the abovementioned metagenomic α proteobacteria invariably contains the gene for Pyruvate:Ferredoxin Oxidoreductase (PFO, Table 1), a key enzyme in the anaerobic metabolism of Clostridiales [36, 37] and also anaerobic eukaryotes . To summarise, we report the first example of α proteobacterial organisms that have all the Hyd maturases required for the assembly and function of [FeFe]-hydrogenase enzymes (Table 1), which often are present with multiple forms in their genome (Table 1).
Uncultivated α proteobacteria possess both major forms of eukaryotic [FeFe]-hydrogenases
In the course of this phylogenetic analysis, we have additionally found consistent clustering of the most divergent type of [FeFe]-hydrogenases, the Nar1 proteins , with the ancestral derivative of type M3 present in R. rubrum (Fig. 2 cf. Additional file 1: Figure S2B). This pattern could be discerned with strong bootstrap support after accurate sequence alignment of phylogenetically diverse proteins that revealed conserved elements shared with type M3 proteins from α proteobacteria (Fig. 2). Of note, Nar1 proteins were previously considered to form the basal branch in phylogenetic trees of [FeFe]-hydrogenases , presumably due to reliance on computer-assisted rather than manually cured sequence alignments for building such trees.
We have searched the latest version of the NCBI websites for proteins and genes in the NR and metagenomic databases using DeltaBLAST , as previously described [32, 46]. Sequence analysis was undertaken by first constructing refined alignments of phylogenetically wide selections of proteins, in some cases combining together proteins belonging to closely related families such as the SAM maturases (see Additional file 1: Figure S1) [10, 32, 33]. Initial sequence alignments were obtained with either MUSCLE or CLUSTALW by routinely using the BLOSUM62 substitution scale and then manually implemented by considering known 3D structures of representative proteins of the orthologous family. See the legend of Fig. 2 and see Additional file 1 for specific details. Such alignments were used to build reference trees with the MEGA 5.2 program  and subsequently refined using known domains and protein motifs from available 3D structures and iteratively implemented until the bootstrap values of nodes containing highly divergent proteins no longer increased. Phylogenetic analysis was then undertaken using, in general, the PhyML program  with the Maximal Likelihood (ML) approach and quantitative estimation of node strength as described . Additional analysis was carried out with Neighbour-Joining (NJ) trees produced with the MEGA 5.2 program or the routine built into blast searches. Analysis of metagenomic data from human gut samples was undertaken as previously described .
Reviewer 1: William Martin
This is a very interesting paper reporting Fe-Fe hydrogenases from alphaproteobacterial genomes that branch as sisters to eukaryotic sequences. This further supports the view that the mitochondrial ancestor was a facultative anaerobe that was capable of mitochondrial type respiration and hydrogenosomal type fermentations. People will reinvestigate the topologies, but the findings reported here are of substantial importance for understanding the evolution of eukaryote physiology. The paper should be published as is.
Reviewer recommendations to authors
I don't see a lot that needs to be done. If people use different models with this data they will get different trees, probably, but the overall message sent by the paper is clear: gene diversity, gene transfer and pangenomes in prokaryotes are at least as important in the eukaryote gene origin issue as hair-splitting and often highly overparameterized single gene phylogenies. There was a nice paper by Ku et al. in PNAS last year talking about how pangenomes figure into the eukaryote gene origin issue. There was also a nice paper by Ku et al. in Nature last year that bears on these issues. Ettema and Gabaldon, the recent Nature papers cited the authors here, apparently still do not understand how LGT affects eukaryote gene origin issues. It is indeed complicated, as Martin Embley and I pointed out in 1998 (Nature) ans as I explained in some detail in 1999 (BioEssays). It is gratifying that microbiologists who understand some physiology, like Mauro Degli Esposti and colleagues, understand the issues that affect the origin of eukaryotic genes from organelle ancestors that live in a world of mosaic prokaryotic chromosomes.
The other referees will surely have a lot to complain about, I am very happy to see these findings.
MDE et al. response: We thank the Reviewer for the very positive comments. In the revised manuscript, we have added the noted reference of Ku et al., Nature 2015 (new Ref. ).
Reviewer 2: Nick Lane
This is a good paper and seems to have been well done. I am not a phylogeneticist so I will defer review of the specific trees to other referees. However, the major conclusions are important, and the paper deserves publication, albeit with some recommended changes and clarifications.
This metagenomic study shows that genes for the two major eukaryotic types of [FeFe] hydrogenase are all present, along with genes for the required maturase enzymes, in the genomes of various alpha-proteobacteria related to Rhodospirillum rubrum. This finding is important in relation to the origin of the eukaryotic cell: was the bacterium that became the mitochondria a facultative anaerobe (in which case it was the ancestor of both hydrogenosomes and aerobic mitochondria) or was it an aerobic bacterium, in which case the [FeFe] hydrogenases were acquired independently on multiple occasions by lateral gene transfer from strictly anaerobic bacteria such as Clostridium? While there are several independent reasons to infer a single acquisition (see below), one problem in the past has been that not all the genes for [FeFe] hydrogenases and the maturases are present in alpha-proteobacteria.
This paper shows that in fact all the required genes are indeed present in close relatives of the facultatively anaerobic bacterium Rhodospirillum rubrum, and hence there is most likely to have been a common origin for aerobic and anaerobic metabolism in the mitochondria and hydrogenosomes. This is a pleasing finding that clarifies a controversial area and is wholly consistent with the predictions of the hydrogen hypothesis (Martin and Muller, Nature 1998), which explicitly predicts that the genes required for hydrogenesis derive from a facultatively anaerobic bacterium that was the common ancestor of both mitochondria and hydrogenosomes. This is also pleasing in that it is entirely consistent with bioenergetic considerations (e.g., Lane and Martin, Nature 2010) which also point to a singular origin of the eukaryotic cell in an endosymbiosis between an archaeon and a bacterium related to modern alpha-proteobacteria. Thus the paper supports the simple hypothesis that eukaryotes arose in a singular endosymbiosis between an archaeaon and a facultatively anaerobic bacterium.
Reviewer recommendations to authors
The major problem that I have with this paper relates to the evolutionary context. In my view the simple phrase 'mitochondria derive from alpha-proteobacteria' is not strictly correct, and could be seriously misleading. The problem is lateral gene transfer, not from bacteria into eukaryotes, but within bacteria (or between bacteria and archaea). The alpha-proteobacteria is a modern group, and they are well known to have evolved mechanisms that drive LGT. Given that the acquisition of mitochondria by an archaeal host cell occurred perhaps 1.5–2 billion years ago, it is not credible to talk about alpha-proteobacteria as if that modern group existed back then almost as it does now. And indeed from Fig. 2 it looks as if there has been some LGT of FeFE hydrogenase genes between different groups of bacteria.
We would therefore predict that many genes that were acquired with the ancestors of mitochondria should NOT branch with the modern alpha-proteobacteria, but rather with an assortment of modern groups. If they had all been acquired from a single endosymbiont then the key prediction is that they should all branch similarly from the base of the eukaryotes, not that they should all be found in modern alpha-proteobacteria. This seems to be the case (e.g., see Ku et al. PNAS 2015 and Ku et al. Nature 2015), although again this is by no means universally agreed. This context is entirely missing from the paper - the emphasis is wholly on the idea that genes for anaerobic metabolism should be found within modern alpha-proteobacteria, and a failure to find them would disprove a singular origin. That is not true. So while it is pleasing to find that they they are in fact common in the alpha-proteobacteria, this should not be couched as a make-or-break finding in the way that it is at several points in the paper.
I also think that Fig. 3 gives a misleading view of the hypothesis presented, and that the claim in the Conclusions for 'a new evolutionary model for [FeFe] hydrogenases…' is not correct and should refer instead far more explicitly to the hydrogen hypothesis, which predicted essentially all of this nearly two decades ago. My specific issue with Fig. 3 is that it makes it look as if the A [FeFe] hydrogenase and M3 [FeFe] hydrogenase were acquired separately in hydrogenosomes rather than via a mitochondrial ancestor which was similar to the alpha Rhodospiralles. The figure should make it clear that the first mitochondria were probably facultatively anaerobic with the same genes as the free-living bacteria, and that hydrogenosomes, anaerobic and aerobic mitochondria all derived from that common ancestor by specific gene loss within particular environments. This does not come across to me from that figure.
I have a few minor issues with some of the citations. For example in the first paragraph of the Background the statement 'originated from a symbiogenic event between an archaea and a metabolically versatile bacterium' is referenced to Sprang et al. and Williams et al. While both these references are appropriate for identifying the host cell as an archaeon, neither paper has anything specific to say about the endosymbiont being 'a metabolically versatile bacterium'. On the contrary - Sprang et al., by implying a phagocytic origin of mitochondria, actually obscures the nature of syntrophy in the endosymbiosis. The authors should cite here the hydrogen hypothesis (Martin and Muller Nature 1998); and on the nature of the host cell should also cite Sousa et al. Nature Microbiol 2016, which shows that Loki is hydrogen-dependent, also as predicted by the hydrogen hypothesis, and consistent with the results presented here.
Finally, as noted above, the paper omits any mention of other approaches to the origin of the eukaryotic cell, for example bioenergetic constraints (see e.g., Lane and Martin Nature 2010, and Lane Cold Spr Harb Pesp Biol 2014 for a discussion). These ideas have been critiqued by Booth and Doolittle PNAS 2015, and Lynch and Marinov PNAS 2015, and answered by Lane and Martin in PNAS 2015 and 2016. Other arguments in favour of a single origin of anaerobic and aerobic metabolism in mitochondria and hydrogenosomes include the very limited and repetitive metabolic repertoire of eukaryotes (equivalent to a single metabolically versatile bacterium; see e.g., Muller et al. Microbiol Moil Biol Rev 2012) and the ocean conditions during the Proterozoic when eukaryotes first arose (see e.g., various papers by Shields, Knoll and Canfield). The point is that there is a broader context than phylogenetics to framing the origin of the eukaryotic cell, and some of this literature should at least be mentioned.
That's all. I repeat, this is a good and interesting paper that is certainly worth publishing, but it would benefit from a broader discussion of the evolutionary context.
MDE et al. response: We thank the Reviewer 2 for the positive comments and constructive criticisms. Our response is as follows.
Regarding further discussion on the broad evolutionary implications of our work, we now state at the end of the revised manuscript that …once the complete genome of Acetobacter CAG:977 will be obtained and analysed in depth, we will be able to further speculate on its relationships with the possible bacterial ancestor of both the aerobic and anaerobic metabolism of eukaryotes. In any case, it now appears to be clear that this ancestor was related to present day Rhodospirillales organisms…
With regard to the relationship between the ancestor of mitochondria and present day alpha proteobacteria, we appreciate the point raised by the Reviewer, which one of us has discussed amply in a paper that is about to be published (and available online - Degli Esposti M. Late Mitochondrial Acquisition, Really? Genome Biol Evol. 2016 Jul 3;8(6):2031-5. doi: 10.1093/gbe/evw130). However, the central problem that our paper is addressing is that previously [FeFe]-hydrogenases and their maturases were considered to be absent, or non functional, in alpha proteobacterial organisms, from which the ancestors of mitochondria have originated - according to the general consensus on the subject. For this reason we think it appropriate to maintain the relatively strong statements regarding the alpha proteobacterial ancestry of mitochondria, citing new references such as the suggested Ku et al. (Nature 2015) to further address the issue. With regard to Fig. 3, we have changed its presentation in the text as a model for the molecular evolution of [FeFe] hydrogenase, modified its graphical layout and changed its legend to better clarify that a single ancestral alpha proteobacterial organism might have transmitted both forms of hydrogenase to the protoeukaryotic cell, as suggested by the Reviewer.
HCP_like, Hybrid Cluster Protein – like domain; LGT, lateral gene transfer; ML, maximum likelihood; MRO, Mitochondria Related Organelles; NJ, neighbour-joining; PFO, Pyruvate:Ferredoxin Oxidoreductase; SSU, Small Subunit
We thank Dr. Paola Bonfante (University of Turin, Italy) for discussion.
This work was sponsored by intramural funds at IIT and by CONACyT grant No. 263876 for the sabbatical research period of MDE in Mexico.
Availability of data and materials
Supporting data are available in the online supplement Additional file 1 and also upon request.
MDE conceived the study and performed all analyses. LL performed the phylogentic analyses. MDE and EMR designed the study. MDE, DC, SR, HBN helped to draft the manuscript and DC refined the final text. All authors read and approved the final manuscript.
Mauro Degli Esposti is Senior Scientist at IIT, via Morego 30, 16136 Genoa, Italy – corresponding Author.
Diego Cortez, Luis Lozano and Esperanza Martinez Romero are members of the academic staff at the Centro de Ciencias Genomicas, Universidad Nacional Autonoma de Mexico (UNAM), Cuernavaca, Morelos, Mexico.
Simon Rasmussen and Henrik Bjørn Nielsen are staff scientists at 3Department of Systems Biology, Center for Biological Sequence Analysis, Technical University of Denmark, Kemitorvet, Building 208, 2800 Kongens Lyngby, Denmark.
The authors declare that they have no competing interests.
Ethics approval and consent to participate
This is not applicable to the present work.
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